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Maternal Nest-Site Choice and Offspring Fitness in a Tropical Snake (Tropidonophis Mairii, Colubridae)

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Maternal Nest-Site Choice and Offspring Fitness in a Tropical Snake (Tropidonophis Mairii, Colubridae) Ecology, 85(6), 2004, pp. 1627±1634 q 2004 by the Ecological Society of America MATERNAL NEST-SITE CHOICE AND OFFSPRING FITNESS IN A TROPICAL SNAKE (TROPIDONOPHIS MAIRII, COLUBRIDAE) G. P. BROWN AND R. SHINE1 Biological Sciences A08, University of Sydney, NSW 2006 Australia Abstract. Do reproducing female reptiles adaptively manipulate phenotypic traits of their offspring by selecting appropriate nest sites? Evidence to support this hypothesis is indirect, mostly involving the distinctive characteristics of used (vs. available) nest sites, and the fact that physical conditions during egg incubation can modify hatchling phenotypic traits that plausibly might in¯uence ®tness. Such data fall well short of demonstrating that nesting females actively select from among potential sites based on cues that predict ®tness- determining phenotypic modi®cations of their offspring. We provide such data from ex- perimental studies on a small oviparous snake (the keelback, Tropidonophis mairii) from the wet-dry tropics of Australia. When presented with a choice of alternative nesting sites, egg-laying females selected more moist substrates for egg deposition. Incubation on wetter substrates signi®cantly increased body size at hatching, a trait under strong positive selection in this population (based on mark±recapture studies of free-ranging hatchlings). Remark- ably, the hydric conditions experienced by an egg in the ®rst few hours after it was laid substantially affected phenotypic traits (notably, muscular strength) of the hatchling that emerged from that egg 10 weeks later. Thus, our data provide empirical support for the hypothesis that nesting female reptiles manipulate the phenotypic traits of their offspring through nest-site selection, in ways that enhance offspring ®tness. Key words: Australia; egg incubation; keelback snake; nest-site selection; offspring ®tness; phe- notypic plasticity; reptile; Tropidonophis mairii. INTRODUCTION natural selection. In the extreme case in which all phe- Within most animal populations, and especially in notypic variation within a cohort of offspring is due to sexually reproducing species, a cohort of neonates dis- environmental, not genetic, factors (as in a clone of plays substantial phenotypic variation. Charles Dar- parthenogens), even intense selection on offspring win's greatest insight was that such variation provides traits will not generate any longer term (evolutionary) an opportunity for natural selection to modify the dis- response because of the absence of genetic variation tribution of ®tness-relevant traits, thereby increasing at the critical loci. This is not to say, however, that the the frequency of characteristics that enhance an organ- system cannot evolve (Via et al. 1995). If speci®c en- ism's probability of surviving and reproducing. The vironmental conditions result in the development of degree to which such selective forces result in evolu- ``®tter'' phenotypic traits, we expect selection for any tionary change within the population depends, how- behaviors that expose the offspring to such environ- ever, upon the proximate mechanisms that generate that ments at the appropriate time within their life history. phenotypic variation. In the simplest case, the pheno- Often, this will involve early development, generally typic variation is engendered entirely by genetic var- the most critical phase because even small deviations iation, so that ®tness differentials will directly modify in early embryos can later cascade through into major underlying gene frequencies. Unfortunately, the reality phenotypic modi®cations as development unfolds (Tan- is more complex. One important complication is the ing 1952, Albon et al. 1983, Henry and Ulijaszek fact that phenotypic variance within a cohort is the 1996). Thus, one of the most important proximate in- result of environmental in¯uences as well as genetic ¯uences on offspring phenotypes may be the conditions factors. Indeed, a high proportion of the quanti®able that eggs experience in natural nests. Minor shifts in variation in many traits is induced by environmental traits such as nest temperatures and water potentials factors, not by genes (Bull 1987, Sultan 1987, War- can have major impacts on phenotypic traits of hatch- kentin 1995, Scheiner and Callahan 1999). lings such as sex, size, shape, color, locomotor ability, This sensitivity of phenotypic traits to environmental and behavior (Burger et al. 1987, Deeming and Fer- conditions has strong implications for the operation of guson 1991, Rhen and Lang 1995). Hence, one major route by which natural selection can modify offspring Manuscript received 13 February 2003; revised 6 October traits in such a system is via genes that control the nest- 2003; accepted 7 October 2003; ®nal version received 31 October site selection behavior of reproducing females (Bull et 2003. Corresponding Editor: D. K. Skelly. 1 Author to whom correspondence should be addressed. al. 1982, Bull 1983, Packard and Packard 1988, Pack- E-mail: [email protected] ard 1991). 1627 1628 G. P. BROWN AND R. SHINE Ecology, Vol. 85, No. 6 Many studies of this topic have been based on rep- Cogger 2000). This species is abundant through many tiles. Laboratory-based experimental work has shown tropical and subtropical areas within the Australasian a high degree of phenotypic plasticity in hatchling rep- region, especially around bodies of water (O'Shea tiles as a result of the conditions experienced during 1991, Cogger 2000), and feeds primarily upon frogs embryogenesis (e.g., Joanen et al. 1987, Ji and Brana (Shine 1991). Keelbacks have been extensively studied 1999, Warner and Andrews 2000, Webb et al. 2001). on the Adelaide River ¯oodplain 60 km east of Darwin Quantitative comparisons of natural nests with avail- in the Australian wet-dry tropics (Webb et al. 2001, able nest sites often reveal substantial differences, pro- Brown and Shine 2002, Brown et al. 2002). Ambient viding strong (albeit indirect) evidence that reproduc- temperatures at this site are high year-round (mean ing females actively select particular types of sites for monthly temperature 27.08C), but precipitation is high- nesting (Muth 1980, Packard and Packard 1988). Last- ly seasonal. More than 78% of the 1394 mm mean ly, ®eld studies suggest that a neonate's phenotype may annual rainfall comes from monsoonal downpours in¯uence its probability of survival (e.g., Fox 1975, within the relatively brief (four-month) ``wet season'' Ferguson and Fox 1984, Arnold and Bennett 1988, Jay- (December±March). Thus, much of the ¯oodplain is ne and Bennett 1990). In combination, these three kinds inundated (and soils in surrounding higher areas are of studies support the hypothesis that mothers may be saturated) during the wet season, but soil moisture lev- able to manipulate the phenotypic traits of their off- els fall gradually over the course of the next several spring by exploiting norms of reaction of reptilian em- months (Shine and Brown 2002). bryogenesis in relation to physical conditions during Keelbacks on the Adelaide River ¯oodplain nest over egg incubation (Beuchat 1986, 1988, Beuchat and Ell- an eight-month period (April±November), with some ner 1987, Shine and Harlow 1996, Arnold and Peterson females producing multiple clutches within the same 2002). That is, some component of selection on off- year (Brown and Shine 2002). Eggs are laid in rela- spring phenotypes in such systems is mediated not tively shallow (,20 cm) burrows in the ¯oodplain soil through differential ®tness of alleles that determine (Shine and Brown 2002). Thus, clutches laid at dif- speci®c offspring traits, but instead through selection ferent times of year experience different hydric con- on genes in females for nest-site selection criteria. ditions during incubation. Experimental studies have Unfortunately, the available evidence remains indi- shown that the phenotypic traits of hatchling keelbacks rect. One problem is that maternal choice among al- are in¯uenced signi®cantly by the physical conditions ternative potential nesting sites has been inferred most- that the eggs experience during incubation. In partic- ly from nonrandom attributes of natural nests rather ular, hatchling phenotypes are affected by the magni- than from experimental studies that manipulate nest tude of diel variation in nest temperatures (Webb et al. availability. Correlational evidence cannot identify the 2001) and by the water potential of the incubation me- actual cue(s) used by nesting females, because so many dium (Shine and Brown 2002). of these cues (e.g., temperature/moisture/soil depth/ type and size of cover object) covary in nature. Ideally, Experimental methods we need to manipulate the array of available nest sites As is true for many species, natural nests of keel- with respect to a speci®c attribute (such as temperature backs are dif®cult to locate (Shine and Brown 2002). or moisture) relevant to the reaction norms of the off- To examine the cues used by nesting females, we cap- spring. Only then can we make a strong link between tured females that had migrated to the wall of Fogg nest-site selection and its impact on offspring pheno- Dam to lay their eggs (Brown and Shine 2002). After types to discern (1) whether or not the female actively the females were measured and weighed, we offered selects among potential nest sites, and if so, (2) which them a choice of potential nest sites differing in hydric cues does she use. We can then (3) examine the impact conditions. Females oviposited 2±18 days after collec- of variation in that cue on hatchling phenotypes, to tion (mean 5 7.7 days). During this period, they were construct a direct causal link between female behavior kept individually in clear plastic cages (40 3 30 3 20 and offspring traits. Lastly, we need ®eld data to (4) cm) with a water bowl and four potential nest sites. explore the ways in which this environmentally in- These were circular black plastic bowls 10 cm in di- duced variation translates into ®tness differentials. Our ameter and 4.5 cm high, covered by a plastic lid with studies on the ecology of snakes in tropical Australia a 3 cm diameter central opening.
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